β2-Adrenergic receptor-dependent sexual dimorphism for murine leukocyte migration

Journal of Neuroimmunology

Volumn 186, Issue 1-2, 2007, Pages 54-62

  de Coupade, Catherine ^a   Brown, Adrienne S ^a   Dazin, Paul F ^a   Levine, Jon D ^a   Green, Paul G ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California San Francisco ^*

Author keywords

2 adrenergic receptor; Adhesion molecules; Knock out mice; Leukocyte recruitment; Sexual dimorphism

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; CELL ADHESION MOLECULE; L SELECTIN; LIPOPOLYSACCHARIDE; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1;

ANIMAL CELL; ARTICLE; CONGENIC STRAIN; CONTROLLED STUDY; FEMALE; INFLAMMATORY DISEASE; KNOCKOUT MOUSE; LEUKOCYTE COUNT; LEUKOCYTE MIGRATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEX DIFFERENCE; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD11A; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; FEMALE; L-SELECTIN; LEUKOCYTES; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, KNOCKOUT; NEUTROPHILS; RECEPTORS, ADRENERGIC, BETA-2; SEX CHARACTERISTICS;

EID: 34248649860     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2007.02.010     Document Type: Article

References (97)

1. Abrass I.B., and Scarpace P.J. Human lymphocyte beta-adrenergic receptors are unaltered with age. J. Gerontol. 36 (1981) 298-301
2. Ajuebor M.N., Swain M.G., and Perretti M. Chemokines as novel therapeutic targets in inflammatory diseases. Biochem. Pharmacol. 63 (2002) 1191-1196
3. Altenburg S.P., Martins M.A., Silva A.R., Cordeiro R.S., and Castro-Faria-Neto H.C. LPS-induced blood neutrophilia is inhibited by alpha 1-adrenoceptor antagonists: a role for catecholamines. J. Leukoc. Biol. 61 (1997) 689-694
4. Amenta F., El-Assouad D., Mignini F., Ricci A., and Tayebati S.K. Neurotransmitter receptor expression by peripheral mononuclear cells: possible marker of neuronal damage by exposure to radiations. Cell. Mol. Biol. 48 (2002) 415-421 (Noisy-le-grand)
5. Ansar Ahmed S., Hissong B.D., Verthelyi D., Donner K., Becker K., and Karpuzoglu-Sahin E. Gender and risk of autoimmune diseases: possible role of estrogenic compounds. Environ. Health Perspect. 107 Suppl 5 (1999) 681-686
6. Barker L.A., Dazin P.F., Levine J.D., and Green P.G. Sympathoadrenal-dependent sexually dimorphic effect of nonhabituating stress on in vivo neutrophil recruitment in the rat. Br. J. Pharmacol. 145 (2005) 872-879
7. Barnes P.J. Beta-adrenergic receptors and their regulation. Am. J. Respir. Crit. Care Med. 152 (1995) 838-860
8. Barnes P.J. Effect of beta-agonists on inflammatory cells. J. Allergy Clin. Immunol. 104 (1999) S10-S17
9. Benschop R.J., Schedlowski M., Wienecke H., Jacobs R., and Schmidt R.E. Adrenergic control of natural killer cell circulation and adhesion. Brain Behav. Immun. 11 (1997) 321-332
10. Bierhaus A., Humpert P.M., and Nawroth P.P. Linking stress to inflammation. Anesthesiol. Clin. 24 (2006) 325-340
11. Bilbo S.D., Dhabhar F.S., Viswanathan K., Saul A., Yellon S.M., and Nelson R.J. Short day lengths augment stress-induced leukocyte trafficking and stress-induced enhancement of skin immune function. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 4067-4072
12. Black P.H. Stress and the inflammatory response: a review of neurogenic inflammation. Brain Behav. Immun. 16 (2002) 622-653
13. Brodde O.E. Endogenous and exogenous regulation of human alpha- and beta-adrenergic receptors. J. Recept. Res. 3 (1983) 151-162
14. Castagnetta L., Granata O.M., Traina A., Cocciadiferro L., Saetta A., Stefano R., Cutolo M., and Carruba G. A role for sex steroids in autoimmune diseases: a working hypothesis and supporting data. Ann. N.Y. Acad. Sci. 966 (2002) 193-203
15. Chen M., Lam B.K., Kanaoka Y., Nigrovic P.A., Audoly L.P., Austen K.F., and Lee D.M. Neutrophil-derived leukotriene B4 is required for inflammatory arthritis. J. Exp. Med. 203 (2006) 837-842
16. Chruscinski A.J., Rohrer D.K., Schauble E., Desai K.H., Bernstein D., and Kobilka B.K. Targeted disruption of the beta2 adrenergic receptor gene. J. Biol. Chem. 274 (1999) 16694-16700
17. Cobelens P.M., Kavelaars A., Vroon A., Ringeling M., van der Zee R., van Eden W., and Heijnen C.J. The beta 2-adrenergic agonist salbutamol potentiates oral induction of tolerance, suppressing adjuvant arthritis and antigen-specific immunity. J. Immunol. 169 (2002) 5028-5035
18. Cutolo M., Sulli A., Pizzorni C., Craviotto C., and Straub R.H. Hypothalamic-pituitary-adrenocortical and gonadal functions in rheumatoid arthritis. In: Sternberg E.M., Haour F.G., and Smith C.C. (Eds). Neuroendocrine and Neural Regulation of Autoimmune and Inflammatory Disease: Molecular, Systems, and Clinical Insights, Annals of the New York Academy of Sciences vol. 992 (2003), New York Academy of Sciences, New York 107-117
19. Da Silva J.A. Sex hormones, glucocorticoids and autoimmunity: facts and hypotheses. Ann. Rheum. Dis. 54 (1995) 6-16
20. Da Silva J.A.P. Sex hormones and glucocorticoids: Interactions with the immune system. In: Cutolo M. (Ed). Neuroendocrine Immune Basis of the Rheumatic Diseases, Annals of the New York Academy of Sciences vol. 876 (1999), New York Academy of Sciences, New York 102-118
21. De Blasi A., Fratelli M., Wielosz M., and Lipartiti M. Regulation of beta adrenergic receptors on rat mononuclear leukocytes by stress: receptor redistribution and down-regulation are altered with aging. J. Pharmacol. Exp. Ther. 240 (1987) 228-233
22. de Coupade C., Gear R.W., Dazin P.F., Sroussi H.Y., Green P.G., and Levine J.D. beta2-Adrenergic receptor regulation of human neutrophil function is sexually dimorphic. Br. J. Pharmacol. 143 (2004) 1033-1041
23. Dhabhar F.S. Stress-induced augmentation of immune function - the role of stress hormones, leukocyte trafficking, and cytokines. Brain Behav. Immun. 16 (2002) 785-798
24. Dina O.A., Aley K.O., Isenberg W., Messing R.O., and Levine J.D. Sex hormones regulate the contribution of PKCepsilon and PKA signalling in inflammatory pain in the rat. Eur. J. Neurosci. 13 (2001) 2227-2233
25. Downing J.E., and Miyan J.A. Neural immunoregulation: emerging roles for nerves in immune homeostasis and disease. Immunol. Today 21 (2000) 281-289
26. Edwards S.W., and Hallett M.B. Seeing the wood for the trees: the forgotten role of neutrophils in rheumatoid arthritis. Immunol. Today 18 (1997) 320-324
27. Elenkov I.J., Wilder R.L., Chrousos G.P., and Vizi E.S. The sympathetic nerve - an integrative interface between two supersystems: the brain and the immune system. Pharmacol. Rev. 52 (2000) 595-638
28. Feldman R.D., Limbird L.E., Nadeau J., Robertson D., and Wood A.J. Alterations in leukocyte beta-receptor affinity with aging. A potential explanation for altered beta-adrenergic sensitivity in the elderly. N. Engl. J. Med. 310 (1984) 815-819
29. Felsner P., Hofer D., Rinner I., Porta S., Korsatko W., and Schauenstein K. Adrenergic suppression of peripheral blood T cell reactivity in the rat is due to activation of peripheral alpha 2-receptors. J. Neuroimmunol. 57 (1995) 27-34
30. Fitzgerald D., Doyle V., Kelly J.G., and O'Malley K. Cardiac sensitivity to isoprenaline, lymphocyte beta-adrenoceptors and age. Clin. Sci. (Lond.) 66 (1984) 697-699
31. Forsythe P., Ebeling C., Gordon J.R., Befus A.D., and Vliagoftis H. Opposing effects of short- and long-term stress on airway inflammation. Am. J. Respir. Crit. Care Med. 169 (2004) 220-226
32. Gaillard R.C., and Spinedi E. Sex- and stress-steroids interactions and the immune system: evidence for a neuroendocrine-immunological sexual dimorphism. Domest. Anim. Endocrinol. 15 (1998) 345-352
33. Garcia J.J., del Carmen Saez M., De la Fuente M., and Ortega E. Regulation of phagocytic process of macrophages by noradrenaline and its end metabolite 4-hydroxy-3-metoxyphenyl-glycol. Role of alpha- and beta-adrenoreceptors. Mol. Cell. Biochem. 254 (2003) 299-304
34. Gietzen D.W., Fregeau D., Goodman T., Weiler P.G., Graf K., and Magliozzi J. Lymphocyte beta-adrenoceptor/effector complex in aging and dementia of the Alzheimer type. Alzheimer Dis. Assoc. Disord. 3 (1989) 132-142
35. Goulding N.J., Euzger H.S., Butt S.K., and Perretti M. Novel pathways for glucocorticoid effects on neutrophils in chronic inflammation. Inflamm. Res. 47 Suppl 3 (1998) S158-S165
36. Green M.S. The male predominance in the incidence of infectious diseases in children: a postulated explanation for disparities in the literature. Int. J. Epidemiol. 21 (1992) 381-386
37. Green P.G., and Levine J.D. Sexual dimorphism in the effect of nonhabituating stress on neurogenic plasma extravasation (2005)
38. Green P.G., Dahlqvist S.R., Isenberg W.M., Strausbaugh H.J., Miao F.J., and Levine J.D. Sex steroid regulation of the inflammatory response: sympathoadrenal dependence in the female rat. J. Neurosci. 19 (1999) 4082-4089
39. Green P.G., Dahlqvist S.R., Isenberg W.M., Miao F.J., and Levine J.D. Role of adrenal medulla in development of sexual dimorphism in inflammation. Eur. J. Neurosci. 14 (2001) 1436-1444
40. Hachicha M., Pouliot M., Petasis N.A., and Serhan C.N. Lipoxin (LX)A4 and aspirin-triggered 15-epi-LXA4 inhibit tumor necrosis factor 1alpha-initiated neutrophil responses and trafficking: regulators of a cytokine-chemokine axis. J. Exp. Med. 189 (1999) 1923-1930
41. Hamilton C.A., Deighton N.M., Jones C.R., and Reid J.L. Changes in rabbit platelet alpha and beta adrenoceptor number and platelet aggregation. Eur. J. Pharmacol. 130 (1986) 145-149
42. Hinojosa-Laborde C., Chapa I., Lange D., and Haywood J.R. Gender differences in sympathetic nervous system regulation. Clin. Exp. Pharmacol. Physiol. 26 (1999) 122-126
43. Hirsch S., and Gordon S. Polymorphic expression of a neutrophil differentiation antigen revealed by monoclonal antibody 7/4. Immunogenetics 18 (1983) 229-239
44. Ignatowski T.A., Kunkel S.L., and Spengler R.N. Interactions between the alpha(2)-adrenergic and the prostaglandin response in the regulation of macrophage-derived tumor necrosis factor. Clin. Immunol. 96 (2000) 44-51
45. Javierre M.Q., Pinto L.V., Lima A.O., and Sassine W.A. Immunologic phagocytosis by macrophages: effect by stimulation of alpha adrenergic receptors. Rev. Bras. Pesqui. Med. Biol. 8 (1975) 271-274
46. Kaposzta R., Tree P., Marodi L., and Gordon S. Characteristics of invasive candidiasis in gamma interferon- and interleukin-4-deficient mice: role of macrophages in host defense against Candida albicans. Infect. Immun. 66 (1998) 1708-1717
47. Kasama T., Miwa Y., Isozaki T., Odai T., Adachi M., and Kunkel S.L. Neutrophil-derived cytokines: potential therapeutic targets in inflammation. Curr Drug Targets Inflamm Allergy 4 (2005) 273-279
48. Kerby J.D., McGwin Jr. G., George R.L., Cross J.A., Chaudry I.H., and Rue III L.W. Sex differences in mortality after burn injury: results of analysis of the National Burn Repository of the American Burn Association. J Burn Care Res 27 (2006) 452-456
49. Kin N.W., and Sanders V.M. It takes nerve to tell T and B cells what to do. J. Leukoc. Biol. 79 (2006) 1093-1104
50. Kohno A., Cinader B., and Seeman P. Age-related changes in beta-adrenoceptors of lymphocytes. Immunol. Lett. 13 (1986) 79-82
51. Krieg Jr. R.J., Thorner M.O., and Evans W.S. Sex differences in beta-adrenergic stimulation of growth hormone secretion in vitro. Endocrinology 119 (1986) 1339-1342
52. Kuhlwein E.C., Irwin M.R., Ziegler M.G., Woods V.L., Kennedy B., and Mills P.J. Propranolol affects stress-induced leukocytosis and cellular adhesion molecule expression. Eur. J. Appl. Physiol. Occup. Physiol. 86 (2001) 135-141
53. Kurokawa Y., Shinkai S., Torii J., Hino S., and Shek P.N. Exercise-induced changes in the expression of surface adhesion molecules on circulating granulocytes and lymphocytes subpopulations. Eur. J. Appl. Physiol. Occup. Physiol. 71 (1995) 245-252
54. Landmann R., Bittiger H., and Buhler F.R. High affinity beta-2-adrenergic receptors in mononuclear leucocytes: similar density in young and old normal subjects. Life Sci. 29 (1981) 1761-1771
55. Landmann R.M., Muller F.B., Perini C., Wesp M., Erne P., and Buhler F.R. Changes of immunoregulatory cells induced by psychological and physical stress: relationship to plasma catecholamines. Clin. Exp. Immunol. 58 (1984) 127-135
56. Liu L., Ridefelt P., Hakansson L., and Venge P. Regulation of human eosinophil migration across lung epithelial monolayers by distinct calcium signaling mechanisms in the two cell types. J. Immunol. 163 (1999) 5649-5655
57. Madden K.S., Sanders V.M., and Felten D.L. Catecholamine influences and sympathetic neural modulation of immune responsiveness. Annu. Rev. Pharmacol. Toxicol. 35 (1995) 417-448
58. Maes M., Van Gastel A., Delmeire L., Kenis G., Bosmans E., and Song C. Platelet alpha2-adrenoceptor density in humans: relationships to stress-induced anxiety, psychasthenic constitution, gender and stress-induced changes in the inflammatory response system. Psychol. Med. 32 (2002) 919-928
59. Maestroni G.J. Sympathetic nervous system influence on the innate immune response. Ann. N.Y. Acad. Sci. 1069 (2006) 195-207
60. Majetschak M., Christensen B., Obertacke U., Waydhas C., Schindler A.E., Nast-Kolb D., and Schade F.U. Sex differences in posttraumatic cytokine release of endotoxin-stimulated whole blood: relationship to the development of severe sepsis. J. Trauma 48 (2000) 832-839 (discussion 839-840)
61. Miles B.A., Lafuse W.P., and Zwilling B.S. Binding of alpha-adrenergic receptors stimulates the anti-mycobacterial activity of murine peritoneal macrophages. J. Neuroimmunol. 71 (1996) 19-24
62. Miles M.P., Leach S.K., Kraemer W.J., Dohi K., Bush J.A., and Mastro A.M. Leukocyte adhesion molecule expression during intense resistance exercise. J. Appl. Physiol. 84 (1998) 1604-1609
63. Miller G.E., and Chen E. Life stress and diminished expression of genes encoding glucocorticoid receptor and beta2-adrenergic receptor in children with asthma. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 5496-5501
64. Mills P.J., Ziegler M.G., Nelesen R.A., and Kennedy B.P. The effects of the menstrual cycle, race, and gender on adrenergic receptors and agonists. Clin. Pharmacol. Ther. 60 (1996) 99-104
65. Mills P.J., Farag N.H., Perez C., and Dimsdale J.E. Peripheral blood mononuclear cell CD62L and CD11a expression and soluble interstitial cell adhesion molecule-1 levels following infused isoproterenol in hypertension. J. Hypertens. 20 (2002) 311-316
66. Mills P.J., Perez C.J., Adler K.A., and Ziegler M.G. The effects of spaceflight on adrenergic receptors and agonists and cell adhesion molecule expression. J. Neuroimmunol. 132 (2002) 173-179
67. Mills P.J., Adler K.A., Dimsdale J.E., Perez C.J., Ziegler M.G., Ancoli-Israel S., Patterson T.L., and Grant I. Vulnerable caregivers of Alzheimer disease patients have a deficit in beta 2-adrenergic receptor sensitivity and density. Am. J. Geriatr. Psychiatry 12 (2004) 281-286
68. Mishra N., Hamilton C.A., Jones C.R., Leslie C., and Reid J.L. Alpha-adrenoceptor changes after oestrogen treatment in platelets and other tissues in female rabbits. Clin. Sci. (Lond.) 69 (1985) 235-238
69. Mohr W., and Menninger H. Polymorphonuclear granulocytes at the pannus-cartilage junction in rheumatoid arthritis. Arthritis Rheum. 23 (1980) 1413-1414
70. Nakamura H., De Rosa S.C., Yodoi J., Holmgren A., Ghezzi P., and Herzenberg L.A. Chronic elevation of plasma thioredoxin: inhibition of chemotaxis and curtailment of life expectancy in AIDS. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 2688-2693
71. O'Hara N., Daul A.E., Fesel R., Siekmann U., and Brodde O.E. Different mechanisms underlying reduced beta 2-adrenoceptor responsiveness in lymphocytes from neonates and old subjects. Mech. Ageing Dev. 31 (1985) 115-122
72. O'Leary E.C., Marder P., and Zuckerman S.H. Glucocorticoid effects in an endotoxin-induced rat pulmonary inflammation model: differential effects on neutrophil influx, integrin expression, and inflammatory mediators. Am. J. Respir. Cell Mol. Biol. 15 (1996) 97-106
73. Oberbeck R. Catecholamines: physiological immunomodulators during health and illness. Curr. Med. Chem. 13 (2006) 1979-1989
74. Parkos C.A. Cell adhesion and migration. I. Neutrophil adhesive interactions with intestinal epithelium. Am. J. Physiol. 273 (1997) G763-G768
75. Pende A., Musso N.R., Vergassola C., Ioverno A., Galbariggi G., and Lotti G. Absence of correlations between plasma catecholamine levels and mononuclear leukocyte beta 2-adrenergic receptors in the elderly. Biomed. Pharmacother. 45 (1991) 383-386
76. Pieri C. Food restriction slows down age-related changes in cell membrane parameters. Ann. N.Y. Acad. Sci. 621 (1991) 353-362
77. Rice P.A., Boehm G.W., Moynihan J.A., Bellinger D.L., and Stevens S.Y. Chemical sympathectomy increases numbers of inflammatory cells in the peritoneum early in murine listeriosis. Brain Behav. Immun. 16 (2002) 654-662
78. Roupe van der Voort C., Heijnen C.J., Wulffraat N., Kuis W., and Kavelaars A. Stress induces increases in IL-6 production by leucocytes of patients with the chronic inflammatory disease juvenile rheumatoid arthritis: a putative role for alpha(1)-adrenergic receptors. J. Neuroimmunol. 110 (2000) 223-229
79. Sanders V.M., Kasprowicz D.J., Swanson-Mungerson M.A., Podojil J.R., and Kohm A.P. Adaptive immunity in mice lacking the beta(2)-adrenergic receptor. Brain Behav. Immun. 17 (2003) 55-67
80. Santos D.R., Calixto J.B., and Souza G.E. Effect of a kinin B2 receptor antagonist on LPS- and cytokine-induced neutrophil migration in rats. Br. J. Pharmacol. 139 (2003) 271-278
81. Sekut L., Champion B.R., Page K., Menius Jr. J.A., and Connolly K.M. Anti-inflammatory activity of salmeterol: down-regulation of cytokine production. Clin. Exp. Immunol. 99 (1995) 461-466
82. Shephard R.J. Adhesion molecules, catecholamines and leucocyte redistribution during and following exercise. Sports Med. 33 (2003) 261-284
83. Spinedi E., Chisari A., Pralong F., and Gaillard R.C. Sexual dimorphism in the mouse hypothalamic-pituitary-adrenal axis function after endotoxin and insulin stresses during development. Neuroimmunomodulation 4 (1997) 77-83
84. Spitzer J.A. Gender differences in some host defense mechanisms. Lupus 8 (1999) 380-383
85. St Pierre Schneider B., Correia L.A., and Cannon J.G. Sex differences in leukocyte invasion in injured murine skeletal muscle. Res. Nurs. Health 22 (1999) 243-250
86. Straub R.H., Westermann J., Scholmerich J., and Falk W. Dialogue between the CNS and the immune system in lymphoid organs. Immunol. Today 19 (1998) 409-413
87. Straub R.H., Linde H.J., Mannel D.N., Scholmerich J., and Falk W. A bacteria-induced switch of sympathetic effector mechanisms augments local inhibition of TNF-alpha and IL-6 secretion in the spleen. FASEB J. 14 (2000) 1380-1388
88. Straub R.H., Mayer M., Kreutz M., Leeb S., Scholmerich J., and Falk W. Neurotransmitters of the sympathetic nerve terminal are powerful chemoattractants for monocytes. J. Leukoc. Biol. 67 (2000) 553-558
89. Tan K.S., McFarlane L.C., and Lipworth B.J. Effect of exogenous female sex-steroid hormones on beta 2-adrenoceptors in healthy males. Eur. J. Clin. Pharmacol. 52 (1997) 281-283
90. Taylor P.R., Brown G.D., Geldhof A.B., Martinez-Pomares L., and Gordon S. Pattern recognition receptors and differentiation antigens define murine myeloid cell heterogeneity ex vivo. Eur. J. Immunol. 33 (2003) 2090-2097
91. Vanscheeuwijck P., Van de Velde E., and Fraeyman N. Characterization of the beta-adrenergic transduction system in spleen mononuclear leukocyte membranes of young and senescent rats. Biochem. Pharmacol. 39 (1990) 2035-2040
92. Varani K., Gessi S., Merighi S., Iannotta V., Cattabriga E., Spisani S., Cadossi R., and Borea P.A. Effect of low frequency electromagnetic fields on A2A adenosine receptors in human neutrophils. Br. J. Pharmacol. 136 (2002) 57-66
93. Veglio F., Tayebati S.K., Schiavone D., Ricci A., Mulatero P., Bronzetti E., Rabbia F., and Amenta F. Alpha1-adrenergic receptor subtypes in peripheral blood lymphocytes of essential hypertensives. J. Hypertens. 19 (2001) 1847-1854
94. Wahle M., Neumann R.P., Moritz F., Krause A., Buttgereit F., and Baerwald C.G. Beta2-adrenergic receptors mediate the differential effects of catecholamines on cytokine production of PBMC. J. Interferon Cytokine Res. 25 (2005) 384-394
95. Wheeldon N.M., Newnham D.M., Coutie W.J., Peters J.A., McDevitt D.G., and Lipworth B.J. Influence of sex-steroid hormones on the regulation of lymphocyte beta 2-adrenoceptors during the menstrual cycle. Br. J. Clin. Pharmacol. 37 (1994) 583-588
96. Whitehead G.S., Walker J.K., Berman K.G., Foster W.M., and Schwartz D.A. Allergen-induced airway disease is mouse strain dependent. Am. J. Physiol., Lung Cell. Mol. Physiol. 285 (2003) L32-L42
97. Wilder R.L., Calandra G.B., Garvin A.J., Wright K.D., and Hansen C.T. Strain and sex variation in the susceptibility to streptococcal cell wall-induced polyarthritis in the rat. Arthritis Rheum. 25 (1982) 1064-1072